Detecting Brain Activity Following a Verbal Command in Patients With Disorders of Consciousness

Background The accurate assessment of patients with disorders of consciousness (DOC) is a challenge to most experienced clinicians. As a potential clinical tool, functional magnetic resonance imaging (fMRI) could detect residual awareness without the need for the patients’ actual motor responses. Methods We adopted a simple active fMRI motor paradigm (hand raising) to detect residual awareness in these patients. Twenty-nine patients were recruited. They met the diagnosis of minimally conscious state (MCS) (male = 6, female = 2; n = 8), vegetative state/unresponsive wakefulness syndrome (VS/UWS) (male = 17, female = 4; n = 21). Results We analyzed the command-following responses for robust evidence of statistically reliable markers of motor execution, similar to those found in 15 healthy controls. Of the 29 patients, four (two MCS, two VS/UWS) could adjust their brain activity to the “hand-raising” command, and they showed activation in motor-related regions (which could not be discovered in the own-name task). Conclusion Longitudinal behavioral assessments showed that, of these four patients, two in a VS/UWS recovered to MCS and one from MCS recovered to MCS+ (i.e., showed command following). In patients with no response to hand raising task, six VS/UWS and three MCS ones showed recovery in follow-up procedure. The simple active fMRI “hand-raising” task can elicit brain activation in patients with DOC, similar to those observed in healthy volunteers. Activity of the motor-related network may be taken as an indicator of high-level cognition that cannot be discerned through conventional behavioral assessment.

[1]  Steven Laureys,et al.  Validation of the Chinese version of the Coma Recovery Scale-Revised (CRS-R) , 2019, Brain injury.

[2]  R. Calabró,et al.  Bridging the Gap Towards Awareness Detection in Disorders of Consciousness: An Experimental Study on the Mirror Neuron System , 2018, Brain Topography.

[3]  Brian L. Edlow,et al.  Functional MRI Motor Imagery Tasks to Detect Command Following in Traumatic Disorders of Consciousness , 2017, Front. Neurol..

[4]  Weiguang Guan,et al.  EEG and fMRI agree: Mental arithmetic is the easiest form of imagery to detect , 2017, Consciousness and Cognition.

[5]  Steven Laureys,et al.  Chinese translation of the Coma Recovery Scale—Revised , 2017, Brain injury.

[6]  N. Latronico Peripheral Causes of Cognitive Motor Dissociation in Patients With Vegetative or Minimally Conscious State. , 2016, JAMA neurology.

[7]  A. Owen,et al.  A hierarchy of event-related potential markers of auditory processing in disorders of consciousness , 2016, NeuroImage: Clinical.

[8]  A. Owen,et al.  The dissociation between command following and communication in disorders of consciousness: an fMRI study in healthy subjects , 2015, Front. Hum. Neurosci..

[9]  A. Comte,et al.  On the difficulty to communicate with fMRI-based protocols used to identify covert awareness , 2015, Neuroscience.

[10]  Steven Laureys,et al.  Cerebral response to subject’s own name showed high prognostic value in traumatic vegetative state , 2015, BMC Medicine.

[11]  Steven Laureys,et al.  Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study , 2014, The Lancet.

[12]  Steven Laureys,et al.  Measuring consciousness in severely damaged brains. , 2014, Annual review of neuroscience.

[13]  A. Owen Disorders of consciousness: Diagnostic accuracy of brain imaging in the vegetative state , 2014, Nature Reviews Neurology.

[14]  Adrian M Owen,et al.  Detecting consciousness: a unique role for neuroimaging. , 2013, Annual review of psychology.

[15]  Catherine J. Stoodley,et al.  The Cerebellum and Cognition: Evidence from Functional Imaging Studies , 2012, The Cerebellum.

[16]  Jeremy D. Schmahmann,et al.  Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study , 2012, NeuroImage.

[17]  Srivas Chennu,et al.  Bedside detection of awareness in the vegetative state: a cohort study , 2011, The Lancet.

[18]  F. Manes,et al.  Functional Imaging Reveals Movement Preparatory Activity in the Vegetative State , 2011, Front. Hum. Neurosci..

[19]  J. Hirsch,et al.  A network approach to assessing cognition in disorders of consciousness , 2010, Neurology.

[20]  Walter G Sannita,et al.  Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome , 2010, BMC medicine.

[21]  M. Boly,et al.  Willful modulation of brain activity in disorders of consciousness. , 2010, The New England journal of medicine.

[22]  Matthew H. Davis,et al.  Towards the routine use of brain imaging to aid the clinical diagnosis of disorders of consciousness. , 2009, Brain : a journal of neurology.

[23]  M. Boly,et al.  Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment , 2009, BMC neurology.

[24]  P. Strick,et al.  Cerebellum and nonmotor function. , 2009, Annual review of neuroscience.

[25]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[26]  Steven Laureys,et al.  When thoughts become action: An fMRI paradigm to study volitional brain activity in non-communicative brain injured patients , 2007, NeuroImage.

[27]  Steven Laureys,et al.  Cerebral response to patient's own name in the vegetative and minimally conscious states , 2007, Neurology.

[28]  J. Giacino,et al.  The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. , 2004, Archives of physical medicine and rehabilitation.

[29]  J. Giacino,et al.  The minimally conscious state: Definition and diagnostic criteria , 2002, Neurology.

[30]  J. Victor,et al.  Power spectra and coherence in the EEG of a vegetative patient with severe asymmetric brain damage , 2000, Clinical Neurophysiology.

[31]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[32]  N. Schiff,et al.  A neuromodulation strategy for rational therapy of complex brain injury states , 2000, Neurological research.

[33]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[34]  R. Malach,et al.  Reaching across the abyss: recent advances in functional magnetic resonance imaging and their potential relevance to disorders of consciousness. , 2009, Progress in brain research.

[35]  Dennis J. L. G. Schutter,et al.  The cerebellum on the rise in human emotion , 2008, The Cerebellum.

[36]  R. Passingham,et al.  Prefrontal interactions reflect future task operations , 2003, Nature Neuroscience.

[37]  D. Shewmon,et al.  The minimally conscious state: definition and diagnostic criteria. , 2002, Neurology.

[38]  N. Schiff,et al.  Diagnosis and treatment of traumatic brain injury. , 2000, JAMA.